Skip to main content
Log in

Fractal dimension based carotid plaque characterization from three-dimensional ultrasound images

  • Original Article
  • Published:
Medical & Biological Engineering & Computing Aims and scope Submit manuscript

Abstract

Irregularity of the plaque surface associated with previous plaque rupture plays an important role in the risk estimation of stroke caused by carotid atherosclerotic lesions. Thus, the aim of this study is to develop and validate novel vulnerability biomarkers from three-dimensional ultrasound (3DUS) images by analyzing the surface morphological characteristics of carotid plaque using fractal geometry features. In the experiments, a total of 38 3DUS plaque images were obtained from two groups of patients treated with 80 mg of atorvastatin or placebo daily for 3 months respectively. Two types of 3D fractal dimensions (FDs) were used to describe the smoothness of plaque surface morphology and the roughness from intensity of 3DUS images. Student’s t test showed that the two fractal features were effective for detecting the statin-related changes in carotid atherosclerosis with p < 0.00023 and p < 0.0113 respectively. It was concluded that the 3D FD measurements were effective for analyzing carotid plaque characteristics and especially effective for evaluating the impact of atorvastatin treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. A VDS (2003) Advanced support vector machines and kernel methods. Neurocomputing 55:5–20

    Article  Google Scholar 

  2. Acharya UR, Subbhuraam VS, Rama M, Molinari F, Saba L, Ho SYS, Ahuja AT, Ho SC, Nicolaides A, Suri J (2012) Atherosclerotic risk stratification strategy for carotid arteries using texture-based features. Ultrasound Med Biol 38:899–915

    Article  Google Scholar 

  3. Ainsworth CD, Blake CC, Tamayo A, Beletsky V, Fenster A, Spence JD (2005) 3D ultrasound measurement of change in carotid plaque volume. Stroke 36:1904–1909

    Article  Google Scholar 

  4. Asvestas P, Golemati S, Matsopoulos G, Nikita K, Nicolaides A (2002) Fractal dimension estimation of carotid atherosclerotic plaques from B-mode ultrasound: a pilot study. Ultrasound Med Biol 28:1129–1136

    Article  Google Scholar 

  5. Awad J, Krasinski A, Parraga G, Fenster A (2010) Texture analysis of carotid artery atherosclerosis from three-dimensional ultrasound images. Med Phys 37:1382–1391

    Article  Google Scholar 

  6. Baber U, Mehran R, Sartori S, Schoos MM, Sillesen H, Muntendam P, Garcia MJ, Gregson J, Pocock S, Falk E, Fuster V (2015) Prevalence, impact, and predictive value of detecting subclinical coronary and carotid atherosclerosis in asymptomatic adults: the BioImage study. J Am Coll Cardiol 65:1065–1074

    Article  Google Scholar 

  7. Backes AR, Eler DM, Minghim R, Bruno OM (2010) Characterizing 3D shapes using fractal dimension. In: Proceedings of the 15th Iberoamerican congress conference on Progress in pattern recognition, image analysis, computer vision, and applications, Brazil

  8. Cardiovascular diseases (2012) World Health Organization. http://www.who.int/mediacentre/factsheets/fs317/en/

  9. Cheng J, Li H, Xiao F, Fenster A, Ding M (2013) Fully automatic plaque segmentation in 3-D carotid ultrasound images. Ultrasound Med Biol 39:3431–3445

    Article  Google Scholar 

  10. Chiu B, Egger M, Parraga G, Fenster A, Spence JD (2006) Quantification of carotid vessel atherosclerosis. In: The processing of the International Society for Optical Engineering

  11. Chiu B, Egger M, Spence JD, Parraga G, Fenster A (2006) Quantification of progression and regression of carotid vessel atherosclerosis using 3D ultrasound images. In: the processing of the 28th International Conference on the IEEE Engineering in Medicine and Biology Society

  12. Chiu B, Egger M, Spence J, Parraga G, Fenster A (2008) Area-preserving flattening maps of 3D ultrasound carotid arteries images. Med Image Anal 12:676–688

    Article  Google Scholar 

  13. Chiu B, Egger M, Spence J, Parraga G, Fenster A (2008) Quantification of carotid vessel wall and plaque thickness change using 3D ultrasound images. Med Phys 35:3691–3710

    Article  Google Scholar 

  14. Chiu B, Beletsky V, Spence J, Parraga G, Fenster A (2009) Analysis of carotid lumen surface morphology using three-dimensional ultrasound imaging. Phys Med Biol 54:1149–1167

    Article  Google Scholar 

  15. Egger M, Spence J, Fenster A, Parraga G (2007) Validation of 3D ultrasound vessel wall volume: an imaging phenotype of carotid atherosclerosis. Ultrasound Med Biol 33:905–914

    Article  Google Scholar 

  16. Elatrozy T, Nicolaides A, Tegos T, Griffin M (1998) The objective characterisation of ultrasonic carotid plaque features. Eur J Vasc Endovasc Surg 16:223–230

    Article  CAS  Google Scholar 

  17. El-Barghouty N, Geroulakos G, Nicolaides A, Androulakis A, Bahal V (1995) Computer assisted carotid plaque characterization. Eur J Vasc Endovasc Surg 9:548–557

    Article  Google Scholar 

  18. Fawcett T (2006) An introduction to ROC analysis. Pattern Recogn Lett 27:861–874

    Article  Google Scholar 

  19. Fenster A, Downey D (2000) 3-D ultrasound imaging. Annu Rev Biomed Eng 2:457–475

    Article  CAS  Google Scholar 

  20. G*Power: Statistical power analyses for Windows and Mac. http://www.gpower.hhu.de/

  21. Gagnepain JJ, Roques-Carmes C (1986) Fractal approach to two dimensional and three dimensional surface roughness. Wear 109:119–126

    Article  Google Scholar 

  22. Hanley J, Mcneil B (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143:29–36

    Article  CAS  Google Scholar 

  23. Homburg PJ, Rozie S, van Gils MJ, van den Bouwhuijsen QJ, Niessen WJ, Dippel DWJ, van der Lugt A (2011) Association between carotid artery plaque ulceration and plaque composition evaluated with multidetector CT angiography. Stroke 42:367–372

    Article  Google Scholar 

  24. Johnsen SH, Mathiesen EB, Joakimsen O, Stensland E, Wilsgaard T, Lochen M-L, Njolstad I, Arnesen E (2007) Carotid atherosclerosis is a stronger predictor of myocardial infarction in women than in men: a 6-year follow-up study of 6226 persons: the Tromso Study. Stroke 38:2873–2880

    Article  Google Scholar 

  25. Kuk M, Wannarong T, Beletsky V, Parraga G, Fenster A, Spence J (2014) Volume of carotid artery ulceration as a predictor of cardiovascular events. Stroke 5:1437–1441

    Article  Google Scholar 

  26. Landry A, Fenster A (2002) Theoretical and experimental quantification of carotid plaque volume measurements made by three-dimensional ultrasound using test phantoms. Med Phys 29

  27. Landry A, Spence JD, Fenster A (2004) Measurement of carotid plaque volume by 3-dimensional ultrasound. Stroke 35:864–869

    Article  Google Scholar 

  28. Landry A, Spence JD, Fenster A (2005) Quantification of carotid plaque volume measurements using 3D ultrasound imaging. Ultrasound Med Biol 31:751–762

    Article  Google Scholar 

  29. Lechareas S, Yanni A, Golemati S, Chatziioannou A, Perrea DN (2016) Ultrasound and biochemical diagnostic tools for the characterization of vulnerable carotid atherosclerotic plaque. Ultrasound Med Biol 42:31–43

    Article  Google Scholar 

  30. Li J-S, Tang Y, Li Z, Li Z (2017) Study on the optical performance of thin-film light-emitting diodes using fractal micro-roughness surface model. Appl Surf Sci 410:60–69

    Article  CAS  Google Scholar 

  31. Lopes R, Betrouni N (2009) Fractal and multifractal analysis: a review. Med Image Anal 13:634–649

    Article  CAS  Google Scholar 

  32. Madani A, Beletsky V, Tamayo A, Munoz C, Spence J (2011) High-risk asymptomatic carotid stenosis: ulceration on 3D ultrasound vs TCD microemboli. Neurology 77:744–750

    Article  CAS  Google Scholar 

  33. Mandelbrot B (1982) The fractal geometry of nature. W. H. Freeman and Company, San Francisco

    Google Scholar 

  34. Militký J, Bajzík V (2001) Surface roughness and fractal dimension. J Text Inst 92:91–113

    Article  Google Scholar 

  35. Naqvi TZ (2015) Quantifying atherosclerosis by 3D ultrasound works!: but there is work to be done. J Am Coll Cardiol 65:1075–1077

    Article  Google Scholar 

  36. Niu L, Qian M, Yang W, Meng L, Xiao Y, Wong K, Abbott D, Liu X, Zheng H (2013) Surface roughness detection of arteries via texture analysis of ultrasound images for early diagnosis of atherosclerosis. PLoS One 8:e76880–e76880

    Article  CAS  Google Scholar 

  37. Paterni EPM (2015) Ultrasound tissue characterization of vulnerable atherosclerotic plaque. Int J Mol Sci 16:10121–10133

    Article  Google Scholar 

  38. Peleg S, Naor J, Hartley R, Avnir D (1984) Multiple resolution texture analysis and classification. IEEE Trans Pattern Anal Mach Intell 6:518–523

    Article  CAS  Google Scholar 

  39. Rothwell P, Gibson R, Warlow C (2000) Interrelation between plaque surface morphology and degree of stenosis on carotid angiograms and the risk of ischemic stroke in patients with symptomatic carotid stenosis. Stroke 31:615–621

    Article  CAS  Google Scholar 

  40. Spence JD, Eliasziw M, DiCicco M, Hackam DG, Galil R, Lohmann T (2002) Carotid plaque area: a tool for targeting and evaluating vascular preventive therapy. Stroke 33:2916–2922

    Article  Google Scholar 

  41. Tsakiris AG, Papanicolaou T (2008) A fractal approach for characterizing microroughness in gravel streams. Arch Hydro Eng Environ Mech 55:29–43

    Google Scholar 

  42. Tsiaparas N, Golemati S, Andreadis I, Stoitsis J, Valavanis I, Nikita K (2011) Comparison of multiresolution features for texture classification of carotid atherosclerosis from B-mode ultrasound. IEEE Trans Inf Technol Biomed 15:130–137

    Article  Google Scholar 

  43. U-King-Im J, Young V, Gillard J (2009) Carotid-artery imaging in the diagnosis and management of patients at risk of stroke. Lancet Neurol 8:569–580

    Article  Google Scholar 

  44. van Engelen A, Wannarong T, Parraga G, Niessen WJ, Fenste A, Spence JD, de Bruijne M (2014) Three-dimensional carotid ultrasound plaque texture predicts vascular events. Stroke 45:2695–2701

    Article  Google Scholar 

  45. van Wesemael B, Poesen J, de Figueiredo T, Govers G (2015) Surface roughness evolution of soils containing rock fragments. Earth Surf Process Landf 21:399–411

    Article  Google Scholar 

  46. Wannarong T, Parraga G, Buchanan D, Fenster A, House AA, Hackam DG, Spence JD (2013) Progression of carotid plaque volume predicts cardiovascular events. Stroke 44:1859–1865

    Article  Google Scholar 

  47. Xie W, Wu Y, Wang W, Zhao D, Liang L, Wang M, Yang Y, Sun J, Shi P, Huo Y (2011) A longitudinal study of carotid plaque and risk of ischemic cardiovascular disease in the Chinese population. J Am Soc Echocardiogr 24:729–737

    Article  Google Scholar 

  48. Yongkang L, Mingyue D (2016) Atorvastatin effect evaluation based on feature combination of three dimension ultrasound images. In: SPIE Medical Imaging, San Diego, California, United States

Download references

Funding

This work was financially supported by the National Nature Science Foundation of China (No. 81571754) and partly supported by the Special Research Fund for the Doctoral Program of Higher Education (No. 20130142130006) and the Innovation Research Foundation of Huazhong University of Science and Technology (No. 2013ZZGH018).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mingyue Ding.

Ethics declarations

Patients provided written informed consent to a study protocol approved by the University of Western Ontario Standing Board of Human Research Ethics.

Appendix: Texture features

Appendix: Texture features

The gray-level co-occurrence matrix included all slices from the 3DUS images. Ten texture measurements were exacted from the co-occurrence matrix in the horizontal, vertical, and diagonal orientations with θ = 0°, 45°, 90°, 135°, including contrast, correlation, dissimilarity, energy, entropy, homogeneity, maximum probability, means, variance, and inverse different moment. For each orientation, the texture measurements were defined as follows:

  1. 1.

    Mean and variance:

$$ \mu =\frac{1}{N}\sum \limits_i\sum \limits_j\sum \limits_kP\left(i,j,k\right) $$
(18)
$$ {\sigma}^2=\frac{1}{N}\sum \limits_i\sum \limits_j\sum \limits_k\left(P\left(i,j,k\right)-\mu \right) $$
(19)
  1. 2.

    Contrast:

$$ Contrast=\sum \limits_i\sum \limits_j\sum \limits_k{\left(\left(i-j\right)\left(i-k\right)\left(j-k\right)\right)}^2P\left(i,j,k\right) $$
(20)
  1. 3.

    Correlation:

$$ Correlation=\frac{\left[\sum \limits_i\sum \limits_j\sum \limits_k\left((ijk)P\right(i,j,k\left)-{\mu}_x{\mu}_y{\mu}_z\right)\right]}{\sigma_x{\sigma}_y{\sigma}_z} $$
(21)
  1. 4.

    Dissimilarity

$$ Dissimilarity=\sum \limits_i\sum \limits_j\sum \limits_k\left[\left|i-j\right|\cdot \left|i-k\right|\cdot \left|j-k\right|\cdot P\left(i,j,k\right)\right] $$
(22)
  1. 5.

    Energy:

$$ Energy=\sum \limits_i\sum \limits_i\sum \limits_k{\left[P\left(i,j,k\right)\right]}^2 $$
(23)
  1. 6.

    Entropy:

$$ Entropy=-\sum \limits_i\sum \limits_j\sum \limits_kP\left(i,j,k\right)\ln P\left(i,j,k\right) $$
(24)
  1. 7.

    Homogeneity

$$ Homogeneity=\sum \limits_i\sum \limits_j\sum \limits_k\frac{P\left(i,j,k\right)}{1+{\left(i-j\right)}^2+{\left(i-k\right)}^2+{\left(j-k\right)}^2} $$
(25)
  1. 8.

    Maximum probability:

$$ maxProbability=\underset{i,j,k}{\max }P\left(i,j,k\right) $$
(26)
  1. 9.

    Inverse different moment:

$$ IDM=\sum \limits_{i,j,k;i\ne j,i\ne k,j\ne k}\frac{P\left(i,j,k\right)}{{\left(i-j\right)}^2+{\left(j-k\right)}^2+{\left(i-k\right)}^2} $$
(27)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, R., Luo, Y., Fenster, A. et al. Fractal dimension based carotid plaque characterization from three-dimensional ultrasound images. Med Biol Eng Comput 57, 135–146 (2019). https://doi.org/10.1007/s11517-018-1865-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-018-1865-5

Keywords

Navigation